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Goniodoris Nodosa REPRODUCTION, LARVAL GROWTH AND METAMORPHOSIS OF THE NUDIBRANCH MOLLUSCS "ONCHIDORIS BILAMELLATA" (L.) AND "GONIODORIS NODOSA" (MONTAGU) Isabel Lafuente A Thesis Submitted for the Degree of PhD at the University of St Andrews 1997 Full metadata for this item is available in St Andrews Research Repository at: http://research-repository.st-andrews.ac.uk/ Please use this identifier to cite or link to this item: http://hdl.handle.net/10023/14641 This item is protected by original copyright Reproduction, Larval Growth and Metamorphosis of the Nudibranch Molluscs Onchidoris bilamellata (L.) and Goniodoris nodosa (Montagu). by Isabel Lafoente Submitted for the Degree of a Master of Philosophy (by research) at the University of St Andrews School of Biological and Medical Sciences September 1996 ProQuest Number: 10167094 All rights reserved INFORMATION TO ALL USERS The quality of this reproduction is dependent upon the quality of the copy submitted. In the unlikely event that the author did not send a complete manuscript and there are missing pages, these will be noted. Also, if material had to be removed, a note will indicate the deletion. uest. ProQuest 10167094 Published by ProQuest LLO (2017). Copyright of the Dissertation is held by the Author. All rights reserved. This work is protected against unauthorized copying under Title 17, United States Code Microform Edition © ProQuest LLO. ProQuest LLO. 789 East Eisenhower Parkway P.Q. Box 1346 Ann Arbor, Ml 48106- 1346 Declaration a) I, Isabel Lafiiente, hereby certify that this thesis has been composed by myself, that it is a record of my own work and that it has not been accepted in partial or complete fulfilment of any other degree or professional qualification. Signed Date b) I was admitted to the Faculty of Science of the University of St Andrews under Ordinance General No. 12 on 1st. April 1990 as a candidate for the degree of Master of Philosophy. 2^ Signed Date c) I hereeb ccrtiff thatt heccndidatehas fflfilied the conditioos of the Resoiutioo and Regulations appropriate to the degree ofMaster nfPhilosophy. Signature of Supervisors Date Date d) Innubmitting this th^s^is so fheUUversiSy of ft Andrews I unde^rand dial I am givivin permission for it to be made available for use in accordance with the regulations of the University Library for the time being in force, subject to any copyright vested in the work not being affected thereby. ACKNOWLEDGEMENTS I am grateful to my supervisors, Christopher Todd and Matthew Bentley for their helpful comments and suggestions in the writing up process, and for their continuous support and advice throughout the fulfilment of this work. I have received invaluable guidance and relevant references from Jose Templado and Marta Calvo to whom I extend my most sincere thanks. I am also truly indebted to my family for their care, concern and encouragement during the course of this degree, and to Fernando Ortega for his priceless help during the writting up and his assistance with some of the figures used in this document; and to Javier Ortega, Jose Moya and Ricardo for their help with the statistics. I am equally thankful to Julian Crowe for his unconditional assistance with computers, and to Joy Baldwin for her warm support and her help with indispensable papers used for this study. I am indebted to UHStAGA, who covered my residence and boarding costs during part of this work. To all the friends I made in St. Andrews, a big thanks, but especially to those from the fencing club, Sandra, Steve, Rasmus, Gareth, Melissa, Rich, Dan, Katie, our coach Derek, and many others; and from the Gatty, Dimitri, Debbie, Helen J., Helen W., Mary A., Mary T., Derek, Bob, Jenny, Richard, Roland, and Pete, thank you for the good times we spent together and your interest in my baby-slugs. I wish not to forget my friends from University Hall, Yoko, Maki, Shazia, Amy, big and small Graham, Lisa, Susanna, Daphne, who were extremely supportive and helpful in times of distress. CONTENTS Page No. CHAPTER 1 GENERAL INTRODUCTION 1 CHAPTER 2 SPAWNING PATTERNS OEONCHIDORISBILAMELLATA L. AND GONIODORIS NODOSA MONTAGU Introduction 6 Materials & Methods Collection, maintenance and mating of tlie adults 9 Experiment 1 9 Experiment 2 11 Experiments 13 Statistical analysis 13 Results Experiment 1 14 Experiment 2 17 Experiment 3 23 Discussion 26 CHAPTER 3 LARVAL GROWTH AND DEVELOPMENT IN ONCHIDORIS BU.AMEU.ATA L. AND GONIODORIS NODOSA MONTAGU Introduction 35 Materials & Methods Collection and maintenance of the adults 37 Spawn mass culture 37 Algal culture 38 Larval culture 39 Statistical analysis 44 Results Onchidoris bilamellata 44 Goniodoris nodosa 49 Discussion 52 CHAPTER 4 INDUCTION OF METAMORPHOSIS IN ONCHIDORIS BILAMELLATA L. AND GONIODORIS NODOSA MONTAGU Introduction 56 Materials & Methods 60 Experiment 1. Potassium ion dose-response of O. bilamellata 64 Experiment 2-4. Induction of metamorphosis in O. bilamellata on contact with and at a distance from the natural prey 64 Experiment 5. Metamorphosis induction of G. nodosa 66 Experiment 6. Delay of metamorphosis in O. bilamellata 66 Statistical analysis 67 Results Experiment 1. Potassium ion dose-response of O. bilamellata 69 Experiment 2-4. Induction of metamorphosis in O. bilamellata on contact with and at a distance from the natural prey 72 Experiment 5. Metamorphosis induction of G. nodosa 76 Experiment 6. Delay of metamorphosis in O. bilamellata 76 Discussion 78 CHAPTER 5 GENERAL DISCUSSION 83 Conclusions 87 REFERENCES 88 ABSTRACT This study investigated the reproduction, larval growth and metamorphosis of the nudibranchs Onchidoris bilamellata (L.) and Goniodoris nodosa (Montagu) under controlled laboratory conditions. In addition, the rare occurrence of spawning events of O. bilamellata taking place in the field outwith the winter and spring reproductive period was studied. Onchidoris bilamellata and Goniodoris nodosa differ in the size and number of eggs produced per spawning event. In the present study O. bilamellata does not exhibit a clear spawning pattern, whereas G. nodosa lays increasingly smaller eggs and larvae as the season progresses. The diameter of the eggs of O. bilamellata is not correlated with the organic content per egg. The data available for G. nodosa were insufficient to analyse this relationship. The rates of larval growth and development are reported for Onchidoris bilamellata and Goniodoris nodosa. These variables do not differ significantly for O. bilamellata between cultures maintained under various light regimes, ranging from continuous darkness to continuous illumination, and are comparable to those of G. nodosa.. The shell growth pattern exhibited by larvae of G nodosa is sigmoid, similar to that of other opisthobranchs. Spawn masses laid during the winter and spring months were collected fresh from the field and compared to spawn masses collected from the field in July and September, outwith the typical spawning period of Onchidoris bilamellata in the British Isles. The shell size of the July and September hatchlings was significantly smaller than that of the winter and spring hatchlings. Furthermore, the larvae hatched from spawn masses laid in September cultured in the laboratory exhibited high mortality rates and the overwhelming majority did not survive through metamorphosis. The significance of the spawning activity of O. bilamellata past the typical spawning period of this species is discussed. The induction of metamorphosis of Onchidoris bilamellata was investigated using seawater containing elevated concentrations of potassium ion, and the results indicate that the optimal concentration inductive of metamorphosis is 19 mM K + ASW. Metamorphosis experiments were also performed with the natural prey of O. bilamellata, the acorn barnacle Semibalanus balanoides (L.). The results suggest that pediveligers can be induced to metamorphose at a distance from the inductive substrata. Attempts were made to identify the natural inductive cue of Goniodoris nodosa, but this was not successful. CHAPTER 1 GENERAL INTRODUCTION Onchidoris bilamellata (L.) and Goniodoris nodosa (Montagu) are intertidal nudibranch molluscs common on the British coasts. O. bilamellata may reach 40 mm in length (Thompson & Brown, 1984), although 25 mm is more usual (Todd, 1979b), and feeds on species of the barnacles Elminius and Chthanalus, but especially Semibalanus (Thompson & Brown, 1984; Chia & Koss, 1988). G. nodosa (Montagu) has a smaller body size, reaching 27 mm in length (Fig. 1.1). In contrast with O. bilamellata, G. nodosa feeds upon encrusting bryozoans, such as Alcyonidium polyoum (Hassall), Callopora dumerili (Audouin) and Flustrellidra hispida (Fabricius) when young, whereas the adults feed preferentially on the ascidians Diplosoma listerianum (Milne Edwards), Botryllus schlosseri (Pallas) and Dendrodoa grossularia (van Beneden) (McMillan, 1942; Miller, 1961; Swennen, 1961). These nudibranchs are primarily found in the intertidal zone in association with their prey items. Onchidoris bilamellata does not extend as high up the shore as its main prey species, Semibalarms balanoides, due to the desiccation risks inherent to this zone (Todd, 1979a), and is frequent in intertidal pools on the undersides of rocks, but it is also common at the lower tidal limit. Goniodoris nodosa is primarily located beneath rocks at the lower limits of the intertidal zone, but may also occur on Fucus sp. fronds on which the polyzoan and ascidian preys settle. Additionally, both of these nudibranchs can also be found subtidally at depths to 120 meters in their northernmost limits of distribution (Ohdner, 1939; Lemche, 1929). The geographic distribution of Onchidoris bilamellata ranges from France to Norway, the White Sea and Spitzbergen, Iceland, Greenland, and the Atlantic and Pacific coasts of North America. Goniodoris nodosa is restricted to north-western Europe, from Norway and the Faeroes to the north west of Spain (Thompson & Brown, 1984). Both of these nudibranchs are common species in Britain. Chapter 1 Page 2 Fig. 1.1. a) Dorsal view of a 14 mm specimen of Onchidoris bilamellata. b) Dorsal view of a 22 mm specimen of Goniodoris nodosa, c) spawn mass of the same attached to the polyzoan Alcyonidium.
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